Unlikely Pairing of Two Alien Species in Oregon Produces Unwanted Offspring

Alfonso Susanna Institut Botànic de Barcelona (IBB-CSIC-ICUB), Pg. del Migdia s/n 08038 Barcelona, Spain Cindy Roché P.O. Box 808 Talent, OR 97540

reat Migrations” are commonly associated with animals. But plants migrate too, and they often use humans,“G who travel, farm, and graze domestic livestock, to expedite long-distance dispersal. These hitch-hikers are usually considered weeds in their new environments. One of the oldest examples, since Neolithic times (Rösch 1998), is cornflower (Centaurea cyanus), so named for its association with cultivated cereal grains. Although the development of herbicides reduced the impact of cornflower on crop yields, other species of Centaurea rank among the worst noncropland weeds in Oregon: yellow starthistle (C. solstitialis), diffuse knapweed (C. diffusa), spotted knapweed (C. stoebe = C. maculosa), squarrose knapweed (C. virgata ssp. squarrosa) and meadow knapweed (C. moncktonii = C. pratensis1) (Roché and Roché 1991). Invasion of new regions brings species together that formerly were seldom (if ever) in close proximity. Sometimes this creates opportunities for hybridization. For example, meadow knapweed, a cross between brown and black knapweed (C. jacea x C. nigra), was been widely known in Europe before it was introduced in North America as a hybrid swarm (a mix of plants that included both parents and hybrids, and hybrid derivatives including F1s, F2s and backcrosses).

An Oregon Centaurea Goes to Barcelona

In 1998, Jeanne Klein (now Standley) collected a “robust and attractive” knapweed with yellow and lavender flowers along the Cow Creek Road while working for the Roseburg District Bureau of Land Management (BLM). The plant that originally caught her eye was a pale and silvery version of meadow knapweed, a weed that was abundant in the area. Besides Holotype of Centaurea x kleinii, collected by Robert Budesa in Curry County, Oregon, housed at the the difference in flower color, she noted that herbarium of the Institut Botànic de Barcelona (BC). 1 Centaurea pratensis Thuill. and C. debeauxii Gren. & Godr. are among “the bracts were different than meadow knapweed,” and she previous names widely used for the hybrid between C. nigra and C. jacea, wondered what species she had stumbled upon. “Most likely but according to Wagenitz (1987), the correct name for this species is C. another noxious weed,” she thought, “but a really pretty one!” moncktonii C. E. Britton. This is also the accepted name in the Flora of North America (Keil and Ochsmann 2006). Some plants had lavender flowers, and some had pale yellow

24 Kalmiopsis Volume 18, 2011 flowers. She couldn’t wait to key it out. When keying didn’t Morphologically, the hybrid is similar to meadow knapweed, but produce results, the mystery deepened. She had noted the adjacent with obvious traces of its yellow starthistle ancestry in floret color, meadow knapweeds and yellow starthistle and began to wonder if shape of the bracts surrounding the flower head, and hairiness of the two had hybridized. That’s when she enlisted the aid of other leaves and stems. botanists. Ken Chambers at the OSU herbarium was stumped. Then, a chance meeting with a BLM manager from the Medford Geographic Origins and Expansion District (Robert Korfhage) provided a connection with his fiancée who had worked with knapweeds at Washington State University. Yellow starthistle is widely distributed along the Mediterranean As luck would have it, Cindy Roché was headed back to Spain to region in its broadest sense, from Iran and Turkey to the complete her post-doctoral research on Crupina. She offered to Iberian Peninsula and North Africa. It originated in the Eastern take pressed specimens to the group in Barcelona that was working Mediterranean, but has expanded to the entire Mediterranean on Centaurea systematics. Another BLM weed specialist, Bob region, usually associated with human disturbance. As an alien Budesa, collected a similar plant on the Rogue River at Quail Creek invader, it has colonized extensive areas in the western US, South (Curry County) and Jeanne found more plants at new locations in America and Australia. Yellow starthistle became established in Douglas County. Last year we published an article describing it as California in the mid-1800s and by 2000 infested more than four a hybrid, honoring Jeanne as the discoverer and using Bob Budesa’s million hectares (Thomsen et al. 1996). It was first reported in collection as the type specimen (Roché and Susanna 2010). Since Oregon in Douglas County in 1914 (Roché and Talbott 1986). then, Barbara Mumblo, botanist with the Forest Service, reported Meadow knapweed is a frequent and fully fertile hybrid between a collection she made of the hybrid in 2006. black knapweed and brown knapweed. Black knapweed is native to the British Isles, with hybrids being common when brown knapweed Against the Odds was introduced from the European continent (Marsden-Jones and Turrill 1954). Ockendon (1975) described the reverse situation The specimens looked like a hybrid between yellow starthistle and in France, suggesting that brown knapweed was native and black meadow knapweed. This combination is entirely unexpected for two knapweed introduced, which is highly questionable following Dostál reasons: these two taxa have incompatible chromosome numbers (1976). Either way, because the F1 hybrid can back-cross with either and are very distantly related, even though both putative parents parent and with other F1 individuals, hybrid swarms normally belong to the large Centaurea Jacea clade (group of close relatives) completely replace the pure forms. Both the parent species and the that stands as the core group of the genus Centaurea (Garcia-Jacas hybrid are common in Eurasia, becoming rare to the East. et al. 2006). Under a geographic classification system, they segregate The earliest reports of meadow knapweed in Oregon date into two different clades. Brown and black knapweed (therefore, to 1911 and 1918 in the Willamette Valley from Portland to meadow) belong to section Jacea, which is in the clade of widely dis- Eugene (Roché and Talbott 1986). Howell (1959) reported tributed species. Centaurea solstitia­ lis belongs to section Mesocentron among the Western Mediterranean group of species (Garcia-Jacas et al. 2006). Thus, meadow knapweed and yellow starthistle are very dis- tant relatives, even though the im- portant characters that define the Centaurea Jacea clade (pollen type “Jacea” and achenes with a double pappus and lateral hilum). The other reason that these two taxa should not cross is the difference in chromosome numbers. Based on multiple counts (Watanabe 2010), meadow knapweed is a tetraploid with 2n = 4x = 44, while yellow starthistle is diploid with 2n = 16. Probability of viable offspring from this incompatible combination should be extremely low. Yet, the apparent hybrid has been found in five separate locations; the distance and lack of seed production indicate that the hybrids arose Distribution of meadow knapweed in Oregon. Map courtesy of Weed Mapper, Oregon Dept. of Agriculture from independent crossings. (http://www.oregon.gov/ODA/PLANT/WEEDS/weedmapper.shtml).

Kalmiopsis Volume 18, 2011 25 that meadow knapweed was cultivated for winter forage near the interior valley lowlands (Umpqua and Willamette Valleys) Roseburg (where it remains abundant today). It is leafier and including both the east slopes of the Coast Range and the west more palatable to livestock than other knapweeds, but as plants slopes of the Cascade Range. In Douglas County the Klamath mature, both palatability and nutritional value decline (Roché Range forms a mountain bridge between the Coast and Cascade and Roché 1991). Ranges; annual precipitation ranges from about 33 inches in the lowland valleys to over 51 inches in the foothills. Substantial Ecological Distribution populations also grow on the mesic eastern slopes and valleys of the Cascade Range near Hood River in the Columbia River Gorge In its native range, yellow starthistle seldom grows in the mountains, in northern Oregon. being restricted to the Mediterranean climate of its origin. In western North America, its distribution is also correlated to Mediterranean With a Little Help From Some Bees? climates, with the most aggressive invasion in California. In the more northern latitudes (e.g., Washington State, ca. 46° to 49° Centaurea species in general are entomophilous (insect pollinated) North), it is restricted to sunny, warm habitats such as south slopes and are visited by a wide range of species for pollen and/or nectar at lower elevations, and despite repeated introductions, does not (Marsden-Jones and Turrill 1954). Each disc floret contains both persist in British Columbia, Canada (Roché and Thill 2001). In male and female flower parts, offering both pollen and nectar. Oregon, it is most competitive in the Mediterranean climate of the To collect these rewards, an insect pushes its proboscis into each inland valleys between the Cascade and Coast Range mountains (a open floret separately. By moving successively across the head, it small, northern extension of the Central Valley of California), the can pollinate many florets by crawling a very short distance, or warm basalt slopes in the Columbia Gorge, and south slopes in the by simply turning. Each floret has one ovule requiring only one foothills of the Blue Mountains. viable and compatible pollen grain to bring about fertilization As its common name suggests, meadow knapweed is a meadow (Marsden-Jones and Turrill 1954). plant, and according to most monographers (e.g., Marsden- Contact between meadow knapweed and yellow starthistle Jones and Turrill 1954, Wagenitz 1987), in the Mediterranean within the range of their native distribution is infrequent because region it grows only in the moistest places in the mountains. In their ecological requirements differ so greatly. What differs in western North America, meadow knapweed extends from coastal southern Oregon is not the biology of the plants, but that appropriate northern California through Oregon and Washington into British habitats occur within flight range of the pollinators. Both species Columbia, primarily in moist forested regions and in meadows, share disturbed sites on roadsides that are adjacent to mesic meadows irrigated pastures, and riparian zones (Roché and Johnson 2003). and riparian zones that support meadow knapweed and warm south- The largest populations of meadow knapweed in Oregon are in facing slopes that are dominated by yellow starthistle.

Is This a New Weed?

The new hybrid is morphologically much closer to meadow knapweed. It is sterile, producing neither seeds nor viable pollen (Carol Mallory-Smith, pers. comm.). In its current form it could show weedy behavior as a perennial herb only through clonal reproduction. Yellow starthistle spreads exclusively by seed, but root and crown fragments of meadow knapweed regrow when disturbed by heavy equipment or cultivation (Roché and Johnson 2003). Alternatively, this sterile hybrid could be one mutation away from becoming a “super weed.” Crupina intermedia is a robust weedy invader that arose when C. crupinastrum (2n = 28) hybridized with C. vulgaris (2n = 30) and subsequently became tetraploid (2n = 4x = 58) (Couderc Distribution of yellow starthistle in Oregon. Map courtesy of Weed Mapper, Oregon Dept. of Agriculture 1975). A parallel scenario for (http://www.oregon.gov/ODA/PLANT/WEEDS/weedmapper.shtml). Centaurea x kleinii could yield a

26 Kalmiopsis Volume 18, 2011 fertile hybrid with exceptional vigor (2n = 4x = 60). Fortunately, co-existence in Oregon for hybrids to appear, but it’s clear that recent surveys indicate that control work by the BLM has been predicting weed behavior in new environments is a dangerous effective in eradicating the hybrid populations. No plants were game. New introductions often experience a lag period before found in 2010 at any of the BLM locations that formerly supported becoming invasive, so erring on the side of prevention is always these hybrids. We don’t know why it took over 100 years of recommended.

Illustration of capitula and phyllary bracts of yellow starthistle, meadow knapweed, and the hybrid between them. Scale: 5 mm in each. Drawings by Carles Puche.

Kalmiopsis Volume 18, 2011 27 Collection Sites References

Curry County: Wild & Scenic Rogue River. Quail Creek. sandy Couderc M. 1975. Origine hybride du Crupina intermedia Briq. loam soil, old roadbed. T33S Rl0W Section 12 SE¼ SW¼. et Cavill. Colloq. Int. C.N.R.S. 235: 531-536. Elevation 400 ft. 42°42’38” N. Lat. 123°49’50” W. Long. Found as Dostál J. 1976. Centaurea L. In: Tutin TG, Heywood VH, Burges single plant, abundant yellow starthistle at site, meadow and diffuse NA, Moore DM, Valentine DH, Walters SM & Webb DA knapweed observed along the river at not too distant locations. (Eds.), Flora Europaea, Vol. 4. Cambridge University Press, Robert Budesa 29 July 2001. London, New York and Melbourne: 254–301. Douglas County: Cow Creek Road, approximately 20 miles Garcia-Jacas N, Uysal T, Romashchenko K, Suárez-Santiago V, southwest of city of Riddle. Growing along roadside between road Ertuğrul K, Susanna A. 2006. Centaurea revisited: a molecular and Cow Creek. Elev. 290 m. 42° 50.303’ N. Lat. 123° 37.204’ survey of the Jacea group. Ann. Bot. (Oxford) 98: 741-753. W. Long. Associated species: Pseudotsuga menziesii, Rubus discolor, Howell JT. 1959. Distributional data on weedy thistles in western Cytisus scoparius, Centaurea pratensis, Centaurea solstitialis, Daucus North America. Leafl. West. Bot. 9: 17-32. carota, Eschscholzia californica, Avena barbata. Jeanne M. Klein; Keil DJ, Ochsmann J. 2006. Centaurea. In: Flora of North America 07 September 2000. Editorial Committee (Eds.), Flora of North America North of Douglas County: Myrtle Island, near Tyee. 43° 28.426’ N Lat. Mexico. Oxford University Press, New York: 181-194. 123° 32.373’ W Long. [T24S R7W Sec. 20] On leading edge of Marsden-Jones EM, Turrill WB. 1954. British Knapweeds: a study the island in cobbles and sandy soil. Elev. 70 m. Associated species: in synthetic taxonomy. London: The Ray Society. Centaurea pratensis, Centaurea solstitialis, Rubus discolor, Chondrilla Ockendon DJ. 1975 Centaurea. In: Stace CA (Ed.), Hybridization juncea. Jeanne Klein & Pete Figura; 20 July 1998. and the flora of the British Islands. Academic Press, London. Douglas County: Island Creek BLM Day Use Area, along 427-428. Cow Creek Road. Elev. 230 m. 42° 54.772’ N. Lat. 123° 28.938’ Roché BF Jr, Roché CT. 1991. Identification, introduction, W. Long. Growing along roadside with Vulpia myuros, Aira distribution, ecology, and economics of Centaurea species. In: caryophyllea, Cynosurus echinatus, Madia sp., Pinus ponderosa, James LF, Evans JO, Ralphs ME, Childs RD (Eds.), Noxious Rubus discolor, Centaurea solstitialis, Centaurea pratensis. Cindy Range Weeds. Westview, Boulder: 274-291. Roché & Jeanne Standley; 28 July 2003. Roché BF Jr, Talbott CJ. 1986. The collection history ofCentaureas Curry County: along Rogue River at west end of Road 250, found in Washington state. Ag. Res. Ctr. Bull. XB0978, northern edge of gravel bar on north bank of river. T35S R13W Washington State University, Pullman. 36 pp. Section 33 SWSW 42°29’59”N. Lat. 124°15’33”W. Long. 100 ft. elev. (From Gold Beach take Road 33 toward Agness, cross over the Rogue River at Lobster Bar and go to Road 3533; continue east ca. 2.5 miles to small road #250). One plant collected. Both Centaurea moncktonii and C. solstitialis in vicinity. Barbara Mumblo #7180601BAM 18 July 2006.

Acknowledgements

Jeanne Standley (BLM Coos Bay District), Bob Budesa (retired, BLM Medford District) and Barbara Mumblo (Rogue River-Siskiyou National Forest) provided information for known sites of the hybrid. Carol Mallory-Smith, Oregon State University, has maintained a small population in cultivation for six years and provided information on infertility. The Oregon Department of Agriculture (Weed Mapper; http://www. oregon.gov/ODA/PLANT/WEEDS/ weedmapper.shtml) provided maps of yellow starthistle and meadow knapweed in Oregon. Carles Puche of the Botanic Institute of Barcelona created the Location of the five collections ofCentaurea x kleinii in Douglas and Curry counties, Oregon. Map prepared wonderful line drawings. by Stephen Meyers, Oregon Flora Project.

28 Kalmiopsis Volume 18, 2011 Roché CT, Johnson DE. 2003. Meadow Knapweed (Centaurea Book Reviews pratensis Thuill.). PNW Ext. Bull. 0566. Oregon State University, Corvallis. 4 pp. Roché CT, Roché BF Jr. 1991. Meadow knapweed invasion in To the Woods: Sinking Roots, Living Lightly, the Pacific Northwest, U.S.A., and British Columbia, Canada. and Finding True Home Northw. Sci. 65: 53-61. Hess, E.S. 2010. Corvallis (OR): Oregon State University Roché CT, Susanna A. 2010. New habitats, new menaces: Press. 175 pp. ISBN 978-087071-581-5. $18.95 Paperback. Centaurea x kleinii (C. moncktonii x C. solstitialis), a new hybrid species between two alien weeds. Collectanea Botanica In 1992, Native Plant Barcelona 29:17-23. Society of Oregon member Roché CT, Thill DC. 2001. Biology of common crupina and Evelyn Hess and her archi­ yellow starthistle, two Mediterranean winter annual invaders tect husband David, both in western North America. Weed Sci. 49: 439-447. in their mid-fifties and Rösch M. 1998. The history of crops and crop weeds in both formerly employed by southwestern Germany from the Neolithic period to modern the University of Oregon, times, as shown by archaeobotanical evidence. Veget. Hist. “… left the toys and noise Archaeobot. 7: 109–125. of urban society for the Thomsen CD, Williams WA, Vayssieres MP, Turner CE, Lanini company of jumping mice, WT. 1996. Yellow starthistle biology and control. Univ. winter wrens, and dark California Pub. 21541, Oakland. nights full of stars and Wagenitz G. 1987. Centaurea. In: Hegi G (Ed.), Illustrierte cricket song …” to live Flora von Mittel-Europa VI, 4. Verlag Paul Parey, Berlin and on 21 logged-off acres in Hamburg: 934-985. the Coast Range foothills Watanabe K. (Accessed 2010). Index to chromosome numbers in south of Eugene. They Asteraceae: http: //www-asteraceae.cla.kobe-u.ac.jp/index. would have “… no house, no electricity, (and) no indoor plumbing …” in this new habitat where they developed a fledgling native plant nursery.To the Woods is Evelyn’s personal Alfonso Susanna is Director account of their fifteen rewarding and challenging years in their of the Botanic Institute of new chosen habitat. Barcelona, Spain. He and Dr. On a special shelf in my bedroom, Evelyn’s book joins two Núria Garcia-Jacas specialize others of the same genre: We Took to the Woods (1942), by Louise in molecular systematics in Dickinson Rich, and Driftwood Valley (1946) by Theodora Asteraceae. As visiting scientists Stanwell Fletcher (reissued by Oregon State University Press in at Washington State University, 1999). All three books were written by women who, with their Pullman, Washington, 1994- husbands, forsook the comforts of modern life to dwell close to Cen­ 1995, they investigated nature and to write accounts of the joys and challenges of their taurea species. Dr. Susanna relationship to the land. I strongly recommend all three to anyone is also editor of the journal, who, like me, has ever dreamed of doing the same. Collectanea Botanica , published Evelyn divides her book into five parts. The first, “The annually (like Kalmiopsis). Alfonso Susanna in a watermelon Setting,” describes the couple’s work on their twenty-one acres pause during his 2009 summer of cut-over Coast Range hillside seventeen miles south of Eugene campaign in Turkey. Cindy Roché, editor of Kal­ while still living in their home near the University of Oregon. miopsis, has a background in Following that introduction, like Driftwood Valley, the book weed science, with an MS from is arranged by seasons: Spring, Summer, Autumn, Winter. As Washington State University on Evelyn states in her Preface, “ … each section records events and the ecology of Centaurea species musings occurring in the specified season from any of the fifteen and a PhD from the University years 1992 to 2007.” of Idaho on the developmental The reader of Evelyn’s account of their lives in the woods will biology of two invasive species marvel at the tenacity of the couple as they developed a plant from the Mediterranean region, nursery in the raw clear-cut environment. Living in a travel trailer Centaurea solstitialis and Crupina with two dogs and a cat but no electricity or indoor plumbing vulgaris. Her post-doctoral proved a challenge even in summer, yet Evelyn clearly remained research at the Botanic Institute enthusiastic and enchanted with their simple life. As the reader will note, she even used an outdoor garbage can as a bathtub. Cindy Roché on Upper Rogue River in Barcelona focused on the Trail, Jackson County, Oregon. Photo origins of several introductions As Evelyn writes, she and her husband “… said good-bye by Robert Korfhage. of Crupina vulgaris. to telephones, television, and electrical appliances …We would make do.” Early on they dug a pond for irrigation. The book’s

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